Host Plant Effects on the Development, Survival, and Reproduction of Dysmicoccus Brevipes (Hemiptera: Pseudococcidae) on Grapevines Author(S): A

Host Plant Effects on the Development, Survival, and Reproduction of Dysmicoccus brevipes (Hemiptera: Pseudococcidae) on Grapevines Author(s): A. Bertin , L. C. Bortoli , M. Botton , and J.R.P. Parra Source: Annals of the Entomological Society of America, 106(5):604-609. 2013. Published By: Entomological Society of America URL: http://www.bioone.org/doi/full/10.1603/AN13030

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. ARTHROPOD BIOLOGY Host Plant Effects on the Development, Survival, and Reproduction of Dysmicoccus brevipes (Hemiptera: Pseudococcidae) on Grapevines

1,2 3 3 1 A. BERTIN, L. C. BORTOLI, M. BOTTON, AND J.R.P. PARRA

Ann. Entomol. Soc. Am. 106(5): 604Ð609 (2013); DOI: http://dx.doi.org/10.1603/AN13030 ABSTRACT Dysmicoccus brevipes (Cockerell, 1893) (Hemiptera: Pseudococcidae) is one of the most frequent and abundant mealybugs in Brazilian vineyards, where it causes direct and indirect damage to the vines. In this study, we investigated the effect of plant structures, cultivars, and vine rootstocks on the development, survival, and reproduction of D. brevipes under laboratory conditions. Leaves of the table- grape cultivar ÔIta´liaÕ (Vitis vinifera) and ÔNia´gara RosadaÕ (Vitis labrusca) and the vine roots of the rootstocks Paulsen 1103 (Vitis berlandieri ϫ V. rupestris) and IAC 572 (Vitis caribaea ϫ 101-14 Mgt) were used as host plants. D. brevipes developed on different vegetative structures, cultivars, and vine rootstocks. D. brevipes showed the shortest developmental period and highest survival and fecundity rates on leaves of cultivar Ita´lia. Survival on leaves was signiÞcantly higher than on roots. Roots of IAC 572 were unsuitable for D. brevipes development, resulting in nonreproductive females. The mealybugsÕ longevity on leaves and vine roots was similar. Higher intrinsic and Þnite rates of increase and net reproductive rate were observed when mealybugs developed on Ita´lia leaves. We concluded that the host plant affects the development and survival of D. brevipes and that the choice of the most appropriate cultivar or vine rootstock can help to reduce pest infestation, and is therefore an additional component to be included in the integrated pest management of grapes.

KEY WORDS mealybug, life cycle, cultivar, rootstock, grape

Mealybugs (Hemiptera: Pseudococcidae) have become The several species of mealybugs associated with increasingly important pests in many crops (BenÐDov grapevines in Brazil include Planococcus citri (Risso, 1994). In vineyards, they are of concern mainly because 1813), Planococcus minor (Maskell, 1897), Pseudococ- of direct infestation of table-grape clusters and indirect cus maritimus (Ehrhorn, 1900), Pseudococcus longispi- damage through virus transmission (Walton and Pringle nus (TargioniÐTozetti, 1867), Pseudococcus viburni 2004; Daane et al. 2008, 2012). Mealybugs can feed on all (Signoret, 1875), and Dysmicoccus brevipes (Cocker- parts of the vine, including the trunk, leaves, and grape ell, 1893) (Daane et al. 2012). clusters, and occasionally on roots (Godfrey et al. 2002, The identiÞcation of D. brevipes occurrence on Daane et al. 2008). Direct loss to production occurs when grapes is relatively new (Morandi Filho, 2008). This mealybugs infest fruits and excrete honeydew that cov- mealybug is primarily a pest of pineapple in Brazil ers the bunches and leaves, resulting in sooty-mold (Silva et al. 1968). On grapes, the species has been growth (Flaherty et al. 1992; Godfrey et al. 2002; Daane mainly found on roots, but it can also infest leaves and et al. 2008, 2012). In wine grapes, the presence of mealy- bunches, causing signiÞcant damage during harvest bugs does not cause economic damage, although some (Daane et al. 2012). No information is available about evidence indicates that they can modify the wine quality the life cycle of D. brevipes on grapes. Given its oc- (Bordeu et al. 2012). However, in table grapes, the pres- currence on roots, this species may be important when ence of mealybugs and the contamination resulting from replanting vineyards, which may lead to reinfestation their feeding can cause cosmetic damage to clusters, and contamination (if this species is also a virus vec- reducing marketability (Godfrey et al. 2002, Gonza´lez tor), as for Pseudococcus calceolariae (Maskell, 1879) and Volosky 2004, Daane et al. 2012). Many mealybug in New Zealand (Bell et al. 2009). In this study, we species can transmit several important grapevine viruses investigated the development, survival, and reproduc- (Cabaleiro and Segura 1997, Golino et al. 2002, Douglas tion of D. brevipes on leaves of two table-grape cul- and Kru¨ger 2008, Bertin et al. 2010), such as the leafroll tivars and roots of two vine rootstocks. viruses, which can reduce productivity and grape quality (Komar et al. 2007). Materials and Methods 1 Department of Entomology and Acarology, University of Sa˜o Maintenance of Insect Colony and Host Plants. A Paulo, 11 Pa´dua Dias Ave., Piracicaba, SP, Brazil 13418-900. colony of D. brevipes was initiated in May 2008 with 2 Corresponding author, e-mail: [email protected]. 3 Laboratory of Entomology, Embrapa Grape and Wine, 515 Livra- adult females originally collected from infested Þg mento St., Bento Gonc¸alves, RS, Brazil 95700-000. roots. The colony was maintained for ϳ15 generations

0013-8746/13/0604Ð0609$04.00/0 ᭧ 2013 Entomological Society of America September 2013 BERTIN ET AL.: BIOLOGICAL ASPECTS OF Dysmicoccus brevipes ON GRAPES 605

on squash (Cabotia´ variety, Cucurbita maxima ϫ Cu- Table 1. Results of statistical analysis for development time curbita moschata) in controlled conditions (25 Ϯ 2ЊC, and longevity of Dysmicoccus brevipes reared on leaves and vine roots of grapes 70 Ϯ 10% relative humidity [RH], and a photoperiod of 14:10 [L:D] h). Traits Test statistic P value The varieties of table grapes that are most com- Leaf or root F (df) monly grown in Brazil were selected for the study. Leaves of the cultivars ÔItaliaÕ (Vitis vinifera) and ÔNia- First instar (development time) 2.85 (1) 0.233 ´ ´ Second instar (development time) 10.03 (1) 0.086 gara RosadaÕ (Vitis labrusca) and the vine rootstocks Third instar (development time) 43.20 (1) 0.022 Paulsen 1103 (Vitis berlandieri ϫ Vitis rupestris) and Nymphal period 19.48 (1) 0.047 IAC 572 (Vitis caribaea ϫ 101-14 Mgt) were used as Longevity 10.41 (1) 0.084 host. The bioassays were conducted by using leaves of adult plants collected in vineyards free from insecti- cide application. The vine rootstocks were cultivated knife resampling (Maia et al. 2000) and were com- in a greenhouse with one plant (1-yr-old) per con- ␣ ϭ tainer (3 liters). pared by using a t-test ( 0.05). Life-table param- Development and Survivorship. To determine the eters for D. brevipes on IAC 572 and Paulsen 1103 roots development time and survival rate of D. brevipes, were not estimated because mealybugs did not pro- adult females from the laboratory colony were isolated duce offspring when reared on IAC 572 roots and there was a low number of reproductive females on in petri dishes (diameter 6.0 cm) with Ita´lia leaf discs (diameter 3.5 cm) until oviposition. First-instar Paulsen 1103 roots. nymphs (Ͻ24-h-old) were transferred to host-plant Development time and adult longevity were ana- leaf discs (diameter 3.5 cm) and vine roots (length 4 lyzed by using nested analysis of variance of the com- cm) in petri dishes (diameter 6 cm) containing a layer bined data set, where leaves and roots were the main (1 cm) of 3% agar-water. In total, 150 nymphs were Þxed factor and the cultivars or rootstocks were the placed individually on leaf discs from each cultivar, random factor nested within leaves/roots. To test for the signiÞcance within groups (leaves or roots), a and 250 nymphs on each root piece of the vine root- ␣ ϭ stock. Mealybugs were transferred to new leaves or t-test was applied ( 0.05) (R Development Core roots every5dtoensure a supply of fresh food. Team 2012). The experiments were conducted in the laboratory The reproductive periods were analyzed with anal- Ϯ Њ Ϯ ysis of variance, followed by TukeyÕs test to separate under controlled conditions at 25 2 C, 70 10% RH, ␣ ϭ and a photoperiod of 14:10 (L:D) h. The progress of the means at 0.05. The effect of host plants on development was checked every 2 d under a binocular survival of immature stages and adult fecundity were microscope and distinguished based on the occur- analyzed Þtting a generalized linear model of the bi- rence of molting exuviae. The survival rate for each nomial and Poisson types, respectively (Nelder and stage is presented as the percentage of individuals that Wedderburn 1972). successfully developed to the next stage. The sex of individual mealybugs could not be determined at the Results egg and Þrst-crawler stages; sex could Þrst be distinguished in the second instar, when males form a co- Development and Survivorship. No D. brevipes coon to complete their development (McKenzie males were observed from Þrst-instar nymphs main- 1967). tained on leaves and roots, indicating the occurrence Reproduction and Longevity. We measured the of thelytokous parthenogenesis. The nymphal stage of longevity and reproductive performance of all insects D. brevipes females consisted of three instars on all that successfully molted to the adult stage in the de- host plants. The development time of the Þrst or sec- velopment/survivorship study. The longevity of adult ond instar did not differ between leaves and rootstocks females was checked every 2 d, and insects were main- (Tables 1 and 2). The greatest differences were obtained individually on leaf discs and vine rootstocks of served in the third instar, with all rootstocks providing each host plant. The number of progeny produced a shorter development time, on average, half the time, from unmated females was recorded, and the nymphs compared with leaves (Tables 1 and 2). laid each day were removed from the leaf or root. The The D. brevipes nymphal period was signiÞcantly duration from adult emergence to oviposition (pre- inßuenced by the host plants, with a shorter devel- reproductive period) and the number of days that the opment time on rootstocks than on leaves (Tables 1 females reproduced (reproductive period) were de- and 2). On leaves, there was a signiÞcant difference termined. The experiments were conducted under the between cultivars, with the longest nymphal period same conditions as previously described. observed on Nia´gara Rosada (Table 2); on roots, the Life Table and Data Analysis. Life-table parameters development period ranged from 31 to 33 d and was for D. brevipes on Ita´lia and Nia´gara Rosada leaves not inßuenced by the rootstock variety. were calculated. These included intrinsic rate of in- The host tissue had a strong effect on D. brevipes ␭ crease (rm), Þnite rate of increase ( ), net reproduc- survival (Table 3). On Ita´lia and Nia´gara Rosada Ͼ tive rate (Ro), mean generation time (TG), and dou- leaves, the survival rate of the Þrst instar was 90%, bling time (DT). The means and standard errors of the reaching almost 100% on Ita´lia. On the vine rootstocks, life-table parameters were estimated based on jack- survival did not exceed 30%. 606 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 106, no. 5

Table 2. Mean number of days (؎SE) for each developmental stage of D. brevipes reared on Ita´lia (Vitis vinifera) and Nia´gara Rosada (Vitis labrusca) table-grape leaves and on Paulsen 1103 (Vitis berlandieri ؋ Vitis rupestris) and IAC 572 (Vitis caribaea ؋ 101-14 Mgt) roots

Vegetative Instars Cultivar or rootstock Nymphal period (n)a structure First (n)a Second (n)a Third (n)a Leaf Ita´lia 13.46 Ϯ 0.48 (144) 12.76 Ϯ 0.56 (135) 17.97 Ϯ 0.79 (85) 42.20 Ϯ 1.07 (82)* Nia´gara Rosada 14.13 Ϯ 0.52 (136) 13.72 Ϯ 0.54 (110) 20.46 Ϯ 1.09 (70) 47.23 Ϯ 1.39 (68)* t (df) Ϫ0.930 (274.95) Ϫ1.22 (241.99) Ϫ1.864 (132.21) Ϫ2.846 (133.34) P value 0.353 0.223 0.064 0.005 Root Paulsen 1103 14.85 Ϯ 0.54 (74) 11.42 Ϯ 0.82 (40) 8.92 Ϯ 1.30 (13) 33.69 Ϯ 1.76 (13) IAC 572 14.25 Ϯ 0.51 (74) 10.25 Ϯ 0.87 (36) 10.40 Ϯ 0.92 (15) 31.43 Ϯ 1.40 (15) t (df) Ϫ0.793 (145.26) Ϫ0.979 (72.95) 0.92 (22.36) Ϫ0.929 (26.25) P value 0.428 0.330 0.366 0.361

Means (Ϯ SE) followed by asterisks were signiÞcantly different at ␣ ϭ 0.05 according to the Student t-test used to perform unpaired comparisons. a Number of individuals observed.

In the second instar, viability differed signiÞcantly for the development of D. brevipes, resulting in non- between Ita´lia and Nia´gara Rosada leaves, with higher reproductive females. survival for mealybugs reared on Ita´lia leaves. Survival Life-Table Parameters. The demographic parame- of second instars on roots did not differ between the ters for D. brevipes differed between the cultivars rootstocks (Table 3). The highest survival in the third Ita´lia and Nia´gara Rosada. The net reproductive rate instar was observed on Ita´lia and Nia´gara Rosada (Ro) that represents the number of times that the leaves, whereas the highest mortality was observed on population increases per generation showed that the Paulsen 1103 roots (Table 3). D. brevipes population increased 20 times per gener- Survival rates from Þrst-instar nymph to adult ation on Ita´lia leaves and Ϸ14 times on Nia´gara Rosada ranged from 5% on roots of Paulsen 1103 to 64% on (Table 5). Ita´lia leaves (Table 3). Despite this low survival on The other life-table parameters were also affected roots, mealybugs that were reared on roots had the by the host plant. Higher values of the intrinsic rate of ␭ shortest developmental period, indicating that the increase (rm) and Þnite rate of increase ( ) were also roots as food source for the species allow D. brevipes observed on Ita´lia leaves (Table 5). The mean gener- development. ation time (TG) was lower for mealybugs reared on Longevity and Reproduction. Female life span on Ita´lia leaves (Table 5), mainly because of the shorter all plants was similar (Table 1). Female longevity on developmental period. Following the same trend, the Ita´lia and Nia´gara Rosada leaves (37.21 Ϯ 1.83 and time required for doubling the population (DT) was 42.52 Ϯ 2.23, respectively) (t ϭϪ1.83; df ϭ 138.06; P Ͼ also shorter on Ita´lia leaves (Table 5). 0.05) as well as on Paulsen 1103 and IAC 572 roots (27.53 Ϯ 5.83 and 18.56 Ϯ 2.30, respectively) (t ϭ Ϫ1.43; df ϭ 15.73; P Ͼ 0.05) was not inßuenced by the Discussion cultivar or rootstock variety. No signiÞcant difference was found in the preovi- Different cultivars and vine rootstocks had a pro- position and oviposition periods between leaves of the nounced effect on the development, survival, and re- two cultivars; however, females reared on Ita´lia leaves production of D. brevipes. This mealybug species showed higher fecundity (Table 4). Fecundity on could develop on leaves and roots of grapevines, al- Paulsen 1103 roots was not included in the statistical though the development time differed between hosts. analysis because of the low number of replicates and The differences observed in the life cycle may be high variance (only four females were reproductively related to nutritional factors, as different plant species active, and the mean number of nymphs per female show differences in nutritional quality that can affect was 57.50 Ϯ 35.33). IAC 572 rootstock was unsuitable insect survival and development.

Table 3. Survival rate (mean ؎ SE, %) for each developmental stage of D. brevipes reared on Ita´lia (V. vinifera) and Nia´gara Rosada V. labrusca) table-grape leaves and on Paulsen 1103 (V. berlandieri ؋ V. rupestris) and IAC 572 (V. caribaea ؋ 101-14 Mgt) roots)

Vegetative Instars Cultivar or rootstock Nymphal period (n)a structure First (n)a Second (n)a Third (n)a Leaf Ita´lia 99.31 Ϯ 0.69a (145) 99.26 Ϯ 0.73a (136) 65.38 Ϯ 4.18ab (130) 63.56 Ϯ 4.23a (129) Nia´gara Rosada 94.44 Ϯ 1.91a (144) 85.93 Ϯ 3.08b (128) 72.16 Ϯ 4.57a (97) 56.55 Ϯ 4.48a (122) Root Paulsen 1103 30.45 Ϯ 2.95b (243) 54.05 Ϯ 5.83c (74) 33.33 Ϯ 7.64c (39) 5.37 Ϯ 1.45b (242) IAC 572 30.45 Ϯ 2.95b (243) 51.42 Ϯ 6.01c (70) 41.66 Ϯ 8.33bc (36) 6.27 Ϯ 1.55b (239)

Means within each column followed by the same letters are not signiÞcantly different (generalized linear model with binomial distribution) according to the CIs. a Number of individuals observed. September 2013 BERTIN ET AL.: BIOLOGICAL ASPECTS OF Dysmicoccus brevipes ON GRAPES 607

؎ Table 4. Duration of preoviposition and oviposition periods (mean ؎ SE, days) and mean number of nymphs per female (mean SE) of female D. brevipes reared on grape leaves and vine roots

Daysb (n)c Vegetative structure Cultivar or rootstocka Fecundityd Preoviposition period Oviposition period Leaf Ita´lia 33.59 Ϯ 1.46a (38) 15.76 Ϯ 0.97a (38) 30.86 Ϯ 2.74a (38) Nia´gara Rosada 35.25 Ϯ 1.16a (38) 19.23 Ϯ 1.18a (38) 24.23 Ϯ 2.02b (38) Root Paulsen 1103 29.00 Ϯ 2.51a (4) 20.25 Ϯ 3.22a (4) Ñe F (df) 1.29 (2) 2.91 (2) Ñ P value 0.282 0.060 0.000

a Females did not oviposit on rootstock IAC 572. b Means within a column followed by the same letters are not signiÞcantly different at ␣ ϭ 0.05 (Tukey test). c Number of individuals observed. d Means within a column followed by the same letters are not signiÞcantly different (GLM with Poisson distribution) according to the conÞdence intervals. e Fecundity on Paulsen 1103 roots was not included in the statistical analysis because of the low number of replicates and high variance (only four females were reproductively active).

The inßuence of the host plant on life-history traits in roots than in leaves, because the vine has the ability has also been demonstrated with other mealybug spe- to store nitrogen in the perennial parts of the plant, cies. The development time of P. citri on grape leaves especially the roots, for subsequent mobilization and (ÔCabernet Sauvignon,Õ ÔIsabel,Õ and Ita´lia) and vine redistribution (Brunetto et al. 2005). roots (Isabel, 101-14, IAC 572) was shorter than that Evidence suggests that high levels of chemical fer- observed on Ita´lia berries (Morandi Filho et al. 2008). tilizers can cause nutritional imbalances in the plant, These authors also observed that P. citri did not com- increasing its susceptibility to insect pressure (Altieri plete its life cycle on IAC 572 roots and produced and Nicholls 2003). Hogendorp et al. (2006) studied infertile adults when reared on Ita´lia berries (Morandi the inßuence of nitrogen concentration on the repro- Filho et al. 2008). duction and development of the citrus mealybug P. The extended nymphal period of D. brevipes on citri on coleus (Solenostemon scutellarioides L. Codd). Nia´gara Rosada leaves may be because of lower nu- Their results showed that higher nitrogen concentra- tritional quality, as a more appropriate food usually tions, in the form of supplemental fertilizers, led to shortens development (Parra 2001), as observed for high reproductive capacity, larger female size, and the development time of the third instar and also for shorter development times. Nitrogen also affected the nymphal period of D. brevipes on both rootstocks. Macrosiphum euphorbiae (Thomas) (Hemiptera: Not all plants or parts of them are nutritionally Aphididae), which when reared on plants without adequate for sap-sucking insects, as in the case of fertilizers or with a low nitrogen level had lower re- mealybugs. The nitrogen content of the host plant is productive performance and longevity, thereby dem- crucial for the development of phytophagous insects, onstrating the importance of this nutrient for insect and the concentration of soluble nitrogen, in the form feeding (Jansson and Ekbom 2002). However, without of free amino acids, can vary according to the species, a quantitative measurement of the nitrogen concen- variety, and part of the plant (Risebrow and Dixon trations in the leaves and vine roots in this study, the 1987). The hypothesis for the shorter developmental effects of nitrogen on the development of D. brevipes time and increased occurrence of this species on roots remain speculative. in the Þeld is that the nitrogen concentration is higher The percentage survival differed between host plants. The low survival on roots may be because of Table 5. Life-table parameters (mean ؎ SE) of D. brevipes antibiosis, when the host plant adversely affects the reared on Ita´lia (V. vinifera) and Nia´gara Rosada (V. labrusca) biology of the phytophagous insect, reducing the size, table-grape leaves longevity, and fecundity and increasing mortality; or alternatively may indicate that this mealybug does not Host plant prefer to feed on roots (Schoonhoven et al. 2005). Nia´gara Parameters Ita´lia (V. P value The age of the host plant can also affect the nutrition Rosada (V. vinifera) labrusca) of phloem sap-sucking insects, owing to physiological changes in plants and in the availability of nutrients Ϯ Ϯ Ͻ Net reproductive 19.82 1.74 13.76 1.13 P 0.0049 (Lazzari and ZontaÐde-Carvalho 2009). Another pos- rate (Ro) Intrinsic rate of 0.037 Ϯ 0.00 0.029 Ϯ 0.00 P Ͻ 0.0000 sibility is that the experiments were conducted in the increase (rm) laboratory, which might be a factor in the low survival Mean generation 80.61 Ϯ 0.54 89.39 Ϯ 0.58 P Ͻ 0.0000 rate. The exposure of the roots in petri dishes may time (TG) Population 18.66 Ϯ 0.62 23.57 Ϯ 0.74 P Ͻ 0.0000 have affected the development of D. brevipes, which doubling time in the Þeld remains protected and covered by the soil. (DT) D. brevipes proved to be able to develop on Ita´lia Ϯ Ϯ Ͻ Finite rate of 1.037 0.00 1.029 0.00 P 0.0000 and Nia´gara Rosada leaves and on IAC 572 and Paulsen increase (␭) 1103 roots. Ita´lia leaves were most suitable for the 608 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 106, no. 5 species development because of the shorter develop- and the IAC 572 rootstock would be an effective strat- mental period combined with higher survival and fe- egy to reduce D. brevipes infestation in the Þeld, cundity, although the development period was shorter whereas the Ita´lia variety and the Paulsen 1103 root- when the mealybugs fed on roots, regardless of the stock tend to favor mealybug infestation. rootstock used. This is consistent with Þeld observa- tions that D. brevipes is the most common species on vine roots in southern Brazil (M.B., unpublished data). Acknowledgments The development period (from Þrst-instar nymph to adult) of D. brevipes on leaves of different pineapple We thank Janet W. Reid (J.W.R. Associates) for English cultivars, its main host plant, was the same as that and technical corrections and the Conselho Nacional de observed on vine roots in this study (SantaÐCecõlia et Desenvolvimento Cientõ´Þco e Tecnolo´gico for granting a ´ scholarship to the Þrst author. al. 2004). However, the survival of D. brevipes on pineapple cultivars (SantaÐCecõ´lia et al. 2004) was lower than the survival rate obtained on the table- grape leaves in this study, suggesting that the host References Cited plant strongly inßuences the species development. Altieri, M. A., and C. I. Nicholls. 2003. Soil fertility manage- Furthermore, in the adult phase, the femalesÕ longev- ment and insect pests: harmonizing soil and plant health ity on table-grape leaves was greater than for D. brevi- in agroecosystems. Soil Till. Res. 72: 203Ð211. pes maintained on different pineapple cultivars Bell, V. A., R.G.E. Bonfiglioni, J.T.S. Walker, P. L. Lo, J. F. (SantaÐCecõ´lia et al. 2004, Colen et al. 2000). Mackay, and S. E. McGregor. 2009. Grapevine leafroll- Regarding reproductive performance, females were associated virus 3 persistence in Vitis vinifera remnant roots. J. Plant Pathol. 91:527Ð533. not able to reproduce on IAC 572 roots. Some vine Ben–Dov, Y. 1994. A systematic catalogue of the mealybugs rootstocks generally show high vigor and resistance to of the world (Insecta: Homoptera: Coccoidea: Pseudo- the main soil pests, including IAC 572, which is resis- coccidae and Putoidae) with data on geographical dis- tant to phylloxera, Daktulosphaira vitifoliae (Fitch, tribution, host plants, biology and economic importance. 1856) (Hemiptera: Phylloxeridae) (Nachtigal 2003). Intercept, Andover, United Kingdom. This resistance may explain the low survival rate and Bertin, S., V. Cavalieri, C. Graziano, and D. 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Bras. The oviposition period was similar on leaves and Fruticultura 27: 110Ð114. vine roots, averaging 32 d. Menezes (1973), studying Cabaleiro, C., and A. Segura. 1997. Field transmission of the D. brevipes life cycle on pineapple, noted that only grapevine leafroll associated virus 3 (GLRaV-3) by the mealybug Planococcus citri. Plant Dis. 81: 283Ð287. fertilized females were able to produce offspring after Colen, K.G.F., L.V.C. Santa–Cecı´lia, J. C. Moraes, and P. B. a preoviposition period of about 8 d. Comparison with Reis. 2000. Efeitos de diferentes temperaturas sobre a the results of this study suggests that the preoviposi- biologia da cochonilha pulverulenta Dysmicoccus brevi- tion period is shorter in females that reproduce sex- pes (Cockerell, 1893) (Hemiptera: Pseudococcidae). ually. Rev. Bras. Fruticultura 22: 248Ð252. Life-table analysis suggested that D. brevipes has a Daane, K. M., M. L. Cooper, S. V. Triapitsyn, V. M. 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